scholarly journals Gut microbiota in the burying beetle, Nicrophorus vespilloides , provide colonization resistance against larval bacterial pathogens

2018 ◽  
Vol 8 (3) ◽  
pp. 1646-1654 ◽  
Author(s):  
Yin Wang ◽  
Daniel E. Rozen
2017 ◽  
Author(s):  
Yin Wang ◽  
Daniel E. Rozen

AbstractCarrion beetles, Nicrophorus vespilloides, are reared on decomposing vertebrate carrion where larvae are exposed to high-density populations of carcass-derived bacteria. We previously showed that larvae do not become colonized with these bacteria, but instead are colonized with the gut microbiome of their parents. These results suggested that bacteria in the beetle microbiome outcompete the carcass derived species for colonization of the larval gut. Here we test this hypothesis directly and quantify the fitness consequences of colonization of the Nicrophorus larval gut with different bacterial symbionts, including the insect pathogen Serratia marcescens. First, we show that beetles colonized by their endogenous microbiome produce significantly heavier broods than those colonized with carcass-bacteria. Next, we show that bacteria from the endogenous microbiome, including Providencia rettgeri and Morganella morganii, are better colonizers of the beetle gut and can outcompete non-endogenous species, including S. marcescens and Escherichia coli, during in vivo competition. Finally, we find that Providencia and Morganella provide beetles with colonization resistance against Serratia and thereby reduce Serratia-induced larval mortality during co-inoculation. Importantly, this effect is eliminated in larvae first colonized by Serratia, suggesting that while competition within the larval gut is strongly determined by priority effects, these effects are less important for Serratia-induced mortality. Our work supports the idea that bacterial gut symbionts provide direct benefits to Nicrophorus larvae by outcompeting potential bacterial pathogens. They further suggest that one benefit of parental care in Nicrophorus vespilloides is the social transmission of the microbiome from caring parents to their offspring.


2017 ◽  
Vol 83 (9) ◽  
Author(s):  
Yin Wang ◽  
Daniel E. Rozen

ABSTRACT Carrion beetles in the genus Nicrophorus rear their offspring on decomposing carcasses where larvae are exposed to a diverse community of decomposer bacteria. Parents coat the carcass with antimicrobial secretions prior to egg hatch (defined as prehatch care) and also feed regurgitated food, and potentially bacteria, to larvae throughout development (defined as full care). Here, we partition the roles of prehatch and posthatch parental care in the transmission and persistence of culturable symbiotic bacteria to larvae. Using three treatment groups (full care, prehatch care only, and no care), we found that larvae receiving full care are predominantly colonized by bacteria resident in the maternal gut while larvae receiving no care are colonized with bacteria from the carcass. More importantly, larvae receiving only prehatch care were also predominantly colonized by maternal bacteria; this result indicates that parental treatment of the carcass, including application of bacteria to the carcass surface, is sufficient to ensure symbiont transfer even in the absence of direct larval feeding. Later in development, we found striking evidence that pupae undergo an aposymbiotic stage, after which they are recolonized at eclosion with bacteria similar to those found on the molted larval cuticle and on the wall of the pupal chamber. Our results clarify the importance of prehatch parental care for symbiont transmission in Nicrophorus vespilloides and suggest that these bacteria successfully outcompete decomposer bacteria during larval and pupal gut colonization. IMPORTANCE Here, we examine the origin and persistence of the culturable gut microbiota of larvae in the burying beetle Nicrophorus vespilloides. This insect is particularly interesting for this study because larvae are reared on decomposing vertebrate carcasses, where they are exposed to high densities of carrion-decomposing microbes. Larvae also receive extensive parental care in the form of carcass preservation and direct larval feeding. We find that parents transmit their gut bacteria to larvae both directly, through regurgitation, and indirectly via their effects on the carcass. In addition, we find that larvae become aposymbiotic during pupation but are recolonized apparently from bacteria shed onto the insect cuticle before adult eclosion. Our results highlight the diverse interactions between insect behavior and development on microbiota composition. They further suggest that competitive interactions mediate the bacterial composition of Nicrophorus larvae together with or apart from the influence of beetle immunity, suggesting that the bacterial communities of these insects may be highly coevolved with those of their host species.


2016 ◽  
Author(s):  
Yin Wang ◽  
Daniel E. Rozen

AbstractCarrion beetles in the genusNicrophorusrear their offspring on decomposing carcasses where larvae are exposed to a diverse microbiome of decomposer bacteria. Parents coat the carcass with antimicrobial secretions prior to egg hatch (defined as Pre-Hatch care) and also feed regurgitated food, and potentially bacteria, to larvae throughout development (defined as Full care). Here we partition the roles of pre- and post-hatch parental care in the transmission and persistence of culturable symbiotic bacteria to larvae. Using three treatment groups (Full-Care, Pre-Hatch care only, and No Care), we found that larvae receiving Full-Care are predominantly colonized by bacteria resident in the maternal gut, while larvae receiving No Care are colonized exclusively with bacteria from the carcass. More importantly, larvae receiving only Pre-Hatch care were also predominantly colonized by maternal bacteria; this result indicates that parental treatment of the carcass, including application of bacteria to the carcass surface, is sufficient to ensure symbiont transfer even in the absence of direct larval feeding. Later in development, we found striking evidence that pupae undergo a aposymbiotic stage, after which they are recolonized at eclosion with bacteria shed in the moulted larval cuticle and on the wall of the pupal chamber. Our results clarify the importance of pre-hatch parental care for symbiont transmission inNicrophorus vespilloides, and suggest that these bacteria successfully outcompete decomposer bacteria during larval and pupal gut colonization.ImportanceHere we examine the origin and persistence of the culturable gut microbiota of larvae in the burying beetleNicrophorus vespilloides.This insect is particularly interesting for this study because larvae are reared on decomposing vertebrate carcasses where they are exposed to high-densities of carrion-decomposing microbes. Larvae also receive extensive parental care in the form of carcass preservation and direct larval feeding. We find that parents transmit their gut bacteria to larvae both directly, through regurgitation, and indirectly via their effects on the carcass. In addition, we find that larvae become aposymbiotic during pupation, but are recolonized from bacteria shed onto the insect cuticle before adult eclosion. Our results highlight the diverse interactions between insect behavior and development on microbiota composition. They further indicate that strong competitive interactions mediate the bacterial composition ofNicrophoruslarvae, suggesting that the bacterial communities of these insects may be highly coevolved with their host species.


2008 ◽  
Vol 20 (1) ◽  
pp. 153-159 ◽  
Author(s):  
Craig A. Walling ◽  
Clare E. Stamper ◽  
Claire L. Salisbury ◽  
Allen J. Moore

mSystems ◽  
2021 ◽  
Author(s):  
Evgenii I. Olekhnovich ◽  
Artem B. Ivanov ◽  
Vladimir I. Ulyantsev ◽  
Elena N. Ilina

We assumed that the enrichment of successful gut microbes by lantibiotic/antibiotic resistance genes can be related to gut microbiota colonization resistance by third-party microbe phenomena and resistance to bacterium-derived or host-derived antimicrobial substances. According to this assumption, competition between the donor-derived and recipient-derived microbes as well as host immunity may play a key role in the FMT-related colonization and redistribution of recipient gut microbiota structure.


2021 ◽  
Vol 118 (48) ◽  
pp. e2102450118
Author(s):  
Ana Duarte ◽  
Darren Rebar ◽  
Allysa C. Hallett ◽  
Benjamin J. M. Jarrett ◽  
Rebecca M. Kilner

Parental care can be partitioned into traits that involve direct engagement with offspring and traits that are expressed as an extended phenotype and influence the developmental environment, such as constructing a nursery. Here, we use experimental evolution to test whether parents can evolve modifications in nursery construction when they are experimentally prevented from supplying care directly to offspring. We exposed replicate experimental populations of burying beetles (Nicrophorus vespilloides) to different regimes of posthatching care by allowing larvae to develop in the presence (Full Care) or absence of parents (No Care). After only 13 generations of experimental evolution, we found an adaptive evolutionary increase in the pace at which parents in the No Care populations converted a dead body into a carrion nest for larvae. Cross-fostering experiments further revealed that No Care larvae performed better on a carrion nest prepared by No Care parents than did Full Care larvae. We conclude that parents construct the nursery environment in relation to their effectiveness at supplying care directly, after offspring are born. When direct care is prevented entirely, they evolve to make compensatory adjustments to the nursery in which their young will develop. The rapid evolutionary change observed in our experiments suggests there is considerable standing genetic variation for parental care traits in natural burying beetle populations—for reasons that remain unclear.


2016 ◽  
Vol 283 (1838) ◽  
pp. 20161023 ◽  
Author(s):  
Natalie Pilakouta ◽  
Per T. Smiseth

A maternal effect is a causal influence of the maternal phenotype on the offspring phenotype over and above any direct effects of genes. There is abundant evidence that maternal effects can have a major impact on offspring fitness. Yet, no previous study has investigated the potential role of maternal effects in influencing the severity of inbreeding depression in the offspring. Inbreeding depression is a reduction in the fitness of inbred offspring relative to outbred offspring. Here, we tested whether maternal effects due to body size alter the magnitude of inbreeding depression in the burying beetle Nicrophorus vespilloides . We found that inbreeding depression in larval survival was more severe for offspring of large females than offspring of small females. This might be due to differences in how small and large females invest in an inbred brood because of their different prospects for future breeding opportunities. To our knowledge, this is the first evidence for a causal effect of the maternal phenotype on the severity of inbreeding depression in the offspring. In natural populations that are subject to inbreeding, maternal effects may drive variation in inbreeding depression and therefore contribute to variation in the strength and direction of selection for inbreeding avoidance.


2018 ◽  
Vol 285 (1881) ◽  
pp. 20180419 ◽  
Author(s):  
Jon Richardson ◽  
Pauline Comin ◽  
Per T. Smiseth

There is growing interest in how environmental conditions, such as resource availability, can modify the severity of inbreeding depression. However, little is known about whether inbreeding depression is also associated with differences in individual decision-making. For example, decisions about how many offspring to produce are often based upon the prevailing environmental conditions, such as resource availability, and getting these decisions wrong may have important fitness consequences for both parents and offspring. We tested for effects of inbreeding on individual decision-making in the burying beetle Nicrophorus vespilloides, which uses the size of a carrion resource to make decisions about number of offspring. Both inbred and outbred females adjusted their initial decisions about number of eggs to lay based on carcass size. However, when we forced individuals to update this initial decision by providing them with a different-sized carcass partway through reproduction, inbred females failed to update their decision about how many larvae to cull. Consequently, inbred females reared too many larvae, resulting in negative fitness consequences in the form of smaller offspring and reduced female post-reproductive condition. Our study provides novel insights into the effects of inbreeding by showing that poor decision-making by inbred individuals can negatively affect fitness.


2018 ◽  
Vol 62 (5) ◽  
Author(s):  
N. J. Ajami ◽  
J. L. Cope ◽  
M. C. Wong ◽  
J. F. Petrosino ◽  
L. Chesnel

ABSTRACT Clostridium difficile infection (CDI), a common cause of hospital-acquired infections, typically occurs after disruption of the normal gut microbiome by broad-spectrum antibiotics. Fidaxomicin is a narrow-spectrum antibiotic that demonstrates a reduced impact on the normal gut microbiota and is approved for the treatment of CDI. To further explore the benefits of this property, we used a murine model to examine the effects of fidaxomicin versus vancomycin on gut microbiota and susceptibility to C. difficile colonization while tracking microbiota recovery over time. Mice were exposed to fidaxomicin or vancomycin by oral gavage for 3 days and subsequently challenged with C. difficile spores at predetermined time points up to 21 days postexposure to antibiotics. Fecal samples were subsequently collected for analysis. Twenty-four hours postchallenge, mice were euthanized and the colon contents harvested. The microbiota was characterized using 16S rRNA gene sequencing. All fidaxomicin-exposed mice (except for one at day 8) were resistant to C. difficile colonization. However, 9 of 15 vancomycin-exposed mice were susceptible to C. difficile colonization until day 12. All vancomycin-exposed mice recovered colonization resistance by day 16. Bacterial diversity was similar prior to antibiotic exposure in both arms and decreased substantially after exposure. A shift in taxonomic structure and composition occurred after both exposures; however, the shift was greater in vancomycin-exposed than in fidaxomicin-exposed mice. In summary, compared with vancomycin, fidaxomicin exposure had less impact on microbiota composition, promoted faster microbial recovery, and had less impact on the loss of C. difficile colonization resistance.


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